Polarity of the ascidian egg cortex and relocalization of cER and mRNAs in the early embryo

• Published in: Journal of cell science Vol. 118; no. 11; pp. 2393 - 2404
• Main Authors: Prodon, François, Dru, Philippe, Roegiers, Fabrice, Sardet, Christian
• Format: Journal Article
• Language: English
• Published: England 01-06-2005
• Subjects: Animals; Biological Evolution; Blastomeres - cytology; Blastomeres - metabolism; Centrosome - metabolism; Cytoskeleton - metabolism; Embryo, Nonmammalian - cytology; Embryo, Nonmammalian - metabolism; Endoplasmic Reticulum, Rough - metabolism; Female; Oocytes - cytology; Oocytes - metabolism; RNA, Messenger, Stored - metabolism; Urochordata - embryology; Zygote - cytology; Zygote - metabolism
• ISSN: 0021-9533; 1477-9137
• DOI: 10.1242/jcs.02366

The mature ascidian oocyte is a large cell containing cytoplasmic and cortical domains polarized along a primary animal-vegetal (a-v) axis. The oocyte cortex is characterized by a gradient distribution of a submembrane monolayer of cortical rough endoplasmic reticulum (cER) and associated maternal postplasmic/PEM mRNAs (cER-mRNA domain). Between fertilization and first cleavage, this cER-mRNA domain is first concentrated vegetally and then relocated towards the posterior pole via microfilament-driven cortical contractions and spermaster-microtubule-driven translocations. The cER-mRNA domain further concentrates in a macroscopic cortical structure called the centrosome attracting body (CAB), which mediates a series of asymmetric divisions starting at the eight-cell stage. This results in the segregation of determinant mRNAs and their products in posterior cells of the embryo precursors of the muscle and germ line. Using two species of ascidians (Ciona intestinalis and Phallusia mammillata), we have pursued and amplified the work initiated in Halocynthia roretzi. We have analysed the cortical reorganizations in whole cells and in cortical fragments isolated from oocytes and from synchronously developing zygotes and embryos. After fertilization, we observe that a cortical patch rich in microfilaments encircles the cER-mRNA domain, concentrated into a cortical cap at the vegetal/contraction pole (indicating the future dorsal pole). Isolated cortices also retain microtubule asters rich in cER (indicating the future posterior pole). Before mitosis, parts of the cER-mRNA domain are detected, together with short microtubules, in isolated posterior (but not anterior) cortices. At the eight-cell stage, the posteriorly located cER-mRNA domain undergoes a cell-cycle-dependant compaction into the CAB. The CAB with embedded centrosomal microtubules can be isolated with cortical fragments from eight-cell-stage embryos. These and previous observations indicate that cytoskeleton-driven repositioning and compaction of a polarized cortical domain made of rough ER is a conserved mechanism used for polarization and segregation of cortical maternal mRNAs in embryos of evolutionarily distant species of ascidians.